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NEUROSURGICAL ANESTHESIOLOGY

The Application of Tetanic Stimulation of the Unilateral Tibial Nerve Before Transcranial Stimulation Can Augment the Amplitudes of Myogenic Motor-Evoked Potentials from the Muscles in the Bilateral Upper and Lower Limbs

Hironobu Hayashi, MD^*, Masahiko Kawaguchi, MD^*, Yuri Yamamoto, MD^*, Satoki Inoue, MD^*, Munehisa Koizumi, MD, Yurito Ueda, MD, Yoshinori Takakura, MD, and Hitoshi Furuya, MD^*

From the Departments of *Anesthesiology, and Orthopaedic Surgery, Nara Medical University, Nara, Japan.

Address correspondence and reprint requests to Masahiko Kawaguchi, MD, Department of Anesthsiology, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8522, Japan. Address e-mail to drjkawa{at}naramed-u.ac.jp.

Abstract

BACKGROUND: Recently, we reported a new technique to augment motor-evoked potentials (MEPs) under general anesthesia, posttetanic MEP (p-MEP), in which tetanic stimulation of the peripheral nerve before transcranial stimulation enlarged amplitudes of MEPs from the muscle innervated by the nerve subjected to tetanic stimulation. In the present study, we tested whether tetanic stimulation of the left tibial nerve can also augment amplitudes of MEPs from the muscles which are not innervated by the nerve subjected to tetanic stimulation.

METHODS: Thirty patients undergoing spinal surgery under propofol-fentanyl anesthesia with partial neuromuscular blockade were examined. For conventional MEP (c-MEP) recording, transcranial stimulation with train-of-five pulses was delivered to C3-4, and the compound muscle action potentials were bilaterally recorded from the abductor pollicis brevis, abductor hallucis (AH), tibialis anterior, and soleus muscles. For p-MEP recording, tetanic stimulation (50 Hz, 50 mA of stimulus intensity) with a duration of 5 s was applied to the left tibial nerve at the ankle 1 s before transcranial stimulation. Transcranial stimulation and recording of compound muscle action potentials were performed in the same manner as c-MEP recording. Amplitudes of c-MEP and p-MEP were compared using Wilcoxon's signed rank test.

RESULTS: Amplitudes of p-MEPs from the left AH muscle innervated by the left tibial nerve with tetanic stimulation were significantly larger compared with those of c-MEPs. Amplitudes of p-MEPs from the bilateral abductor pollicis brevis and soleus muscles and right AH and tibialis anterior muscles, which were not innervated by the left tibial nerve with tetanic stimulation, were also significantly larger compared with those of c-MEPs.

CONCLUSION: In patients under propofol and fentanyl anesthesia with partial neuromuscular blockade, the application of tetanic stimulation to the left tibial nerve augmented the amplitudes of MEPs from the muscles without tetanic nerve stimulation and those with stimulation.

Intraoperative monitoring of myogenic motor-evoked potential (MEP) to transcranial stimulation of the motor cortex has become a commonly used technique for the early detection and reversal of spinal cord injury during operations in which there is a risk for spinal cord injury.1–3 However, clinical and experimental use of these techniques has shown that the elicited responses are very sensitive to suppression by most anesthetics and muscular blockade.4–10 Furthermore, patients with preoperative neuropathy, such as spinal cord tumor, Chiari malformation, and scoliosis, may have very poor baseline MEPs. Although multipulse stimulation setups have been proposed to improve monitoring reliability,11–13 further improvements in the technique for reliable MEP recording would be helpful.

We reported a new technique for MEP recording, called posttetanic MEP (p-MEP) (Fig. 1), in which MEP amplitude can be enlarged by tetanic stimulation of the peripheral nerve before transcranial stimulation, compared with that of conventional MEP (c-MEP).14 Using this technique, we can successfully enlarge MEP amplitudes under general anesthesia with partial neuromuscular blockade. Originally, we proposed that MEP augmentation by tetanic stimulation of the peripheral nerve might be limited in the muscles innervated by the peripheral nerve with tetanic stimulation (TS-muscle). For example, tetanic stimulation of the left tibial nerve was considered to augment only the muscles innervated by that nerve, including the left abductor hallucis (AH) muscle, but not other muscles, which are not innervated by the left tibial nerve. However, we unexpectedly found that tetanic stimulation of the peripheral nerve at one site also augmented MEP amplitudes from other muscles which are not innervated by the nerve with tetanic stimulation (non-TS muscles). To our knowledge, this is the first report to show that tetanic stimulation of the peripheral nerve at one site can augment MEP amplitudes not only from TS muscle, but also from non-TS muscles. The present study was therefore conducted to investigate whether tetanic stimulation of the left tibial nerve can augment MEP amplitude from the non-TS muscles, including the bilateral abductor pollicis brevis (APB), tibialis anterior (TA), and soleus (S) muscles and the right AH muscle.

View larger version (18K): [in this window] [in a new window]   Figure 1. Technique to record posttetanic motor-evoked potential (p-MEP) and conventional MEP (c-MEP). For c-MEP recording, transcranial stimulation was performed by train-of-five pulses with an interstimulus interval of 2 ms to C3 and C4 (international 10–20 System) and the compound muscle action potentials were recorded. For p-MEP recording, tetanic stimulation of the left tibial nerve with a duration of 5 s and a stimulus intensity of 50 mA at 50 Hz was performed before transcranial stimulation with a posttetanic interval of 1 s.

METHODS

After Institutional approval at Nara Medical University, Nara, Japan, written informed consent was obtained from each patient. Thirty patients undergoing elective spine and spinal cord surgery at Nara Medical University, Nara, Japan, were enrolled in the study. Patients ranged in age from 17 to 85 yr (mean 58 yr). There were 15 men and 15 women. Disease in these patients included cervical spinal stenosis (n = 6), cervical spinal tumor (n = 4), lumber spinal stenosis (n = 13), lumber spinal tumor (n = 4), and others (n = 3). Patients with preoperative motor dysfunction, seizures, implanted atrial or ventricular pacemakers, or other implanted neural stimulators or pumps were excluded. Patients with moderate to severe sensory deficits were also excluded from the study, whereas patients with mild sensory deficits, including numbness and intermittent claudication, were included. Anesthesia was standardized in all patients. No premedication was given before anesthesia, which was induced with 2–4 µg/kg of fentanyl, 0.1–0.15 mg/kg of vecuronium and propofol. Target-controlled infusion was used for propofol administration at a target plasma concentration of 4–6 µg/mL. Anesthesia was maintained using a regimen of propofol and fentanyl with neuromuscular blockade. Propofol was maintained at a target plasma concentration of 3–5 µg/mL. After the trachea was intubated, the lungs were ventilated mechanically to maintain the partial pressure of end-tidal carbon dioxide between 30 and 40 mm Hg. A mixture of air and oxygen at a fractional inspired concentration of 40%–50% was administered. Fentanyl was administered for pain relief as required to mitigate heart rate and arterial blood pressure increase. Rectal temperature was maintained between 35.5°C and 37.0°C. The level of neuromuscular blockade was assessed by the M-response from the APB muscle in response to electrical stimulation of the median nerve at 50 mA. Twitch height of the M-response was maintained at a level of 2–5 mV by a continuous administration of vecuronium at 0.04–0.06 mg · kg^–1 · h^–1.

Techniques for c-MEP and p-MEP Recording
c-MEP
Multipulse transcranial electric stimulation was performed using a multipulse stimulator (D-185; Digitimer, Welwyn Garden City, United Kingdom). A train-of-five pulses stimulation was delivered at 2 ms interstimulus intervals (500 Hz). The stimulating electrodes consisted of a pair of 14.5 mm silver-plated disk electrodes at C3 (cathode) and C4 (anode) (international 10–20 System) affixed with conductive paste. The stimulus intensity of transcranial stimulation was determined at the beginning of MEP recording as supramaximal (approximately 500 V). The compound muscle action potentials were bilaterally recorded from the skin over the APB, AH, TA, and S muscles. A ground electrode was placed on the left or right arm proximal to the elbow. Evoked myographic responses were amplified with a 0.3–3-kHz bandpass filter. An intraoperative MEP measurement system (Neuropack MEB-2208; Nihon Koden, Tokyo, Japan) was used for MEP monitoring.

p-MEP
Tetanic stimulation (50 Hz, 50 mA of stimulus intensity) with a duration of 5 s was applied to the left tibial nerve, which innervates the left AH muscle, at the ankle 1 s before transcranial electric stimulation. Transcranial electric stimulation was automatically triggered after the application of tetanic stimulation. Transcranial electrical stimulation was performed in the same manner mentioned in c-MEP recording. The compound muscle action potentials were recorded from the same muscles as c-MEP recording.

Study Protocol
Assessments of c-MEPs and p-MEPs were performed before any surgical interventions that might have resulted in impaired spinal cord functioning. First, control c-MEPs were recorded. Then p-MEPs were recorded. In our preliminary study, we determined that a 2-min interval after p-MEP recording did not affect subsequent MEP responses, so that an interval of p-MEP recordings was set at more than 2 min. Peak-to-peak amplitude was determined from the average of two individual responses. When the average MEP amplitude was <30 µV, the MEP response was defined as "no response." Because the left tibial nerve at the ankle mainly innervates the left AH muscle, but not other muscles used in this study, we defined left AH muscle as "TS muscle" and bilateral APB, TA, and S muscles and right AH muscles as "non-TS muscles."

Statistical Analysis
Sample size in the current study was determined based on the data in our previous and preliminary studies. We assumed that it was clinically important that MEP amplitude was augmented by 75% after the application of tetanic stimulation of the peripheral nerve. Based on the formula for normal theory and assuming a Type I error of 0.05 and a power of 0.8, 30 patients were required for each comparison. Comparisons of amplitudes of c-MEP and p-MEP at each recording site were performed using Wilcoxon's signed rank test. P < 0.05 was considered significant.

RESULTS

There were no complaints of seizures or skin burns postoperatively. Success rates of MEP recording from all muscles are shown in Table 1. MEP amplitudes from all recording sites could be obtained reliably in 24 of 30 patients (80%) by c-MEP, and 29 of 30 patients (97%) by p-MEP. The patients without reliable MEP responses by p-MEP also had no reliable responses by c-MEP.

Comparisons of amplitudes of c-MEP and p-MEP are shown in a box plot (Fig. 2). MEP amplitude from the left AH muscle (TS muscle) was significantly increased by the application of tetanic stimulation to the left tibial nerve compared with that of c-MEP. Similarly, MEP amplitudes from the bilateral APB, right AH, right TA, and bilateral S muscles (non-TS muscles) were significantly increased by the application of tetanic stimulation to the left tibial nerve compared with that of c-MEP. Only MEP amplitude from the left TA muscle (non TS muscle) was not significantly augmented by p-MEP, although MEP amplitude tended to increase with a P value of 0.0532. The representative c-MEP and p-MEP recordings of the same patient are shown in Figure 3. Note that MEP amplitudes from the bilateral APB, AH, TA, and S muscles were increased after the application of tetanic stimulation to the left tibial nerve.

View larger version (17K): [in this window] [in a new window]   Figure 2. Comparisons of amplitudes of conventional motor-evoked potential (c-MEPs) and posttetanic MEP (p-MEPs) from the bilateral abductor pollicis brevis (APB), abductor hallucis (AH), tibialis anterior (TA), and soleus (S) muscles. For p-MEP recording, tetanic stimulation of the left tibial nerve at the ankle with a duration of 5 s and a stimulus intensity of 50 mA at 50 Hz was performed before transcranial stimulation with a posttetanic interval of 1 s. Because the left tibial nerve mainly innervates the left AH muscle, but not other muscles, the left AH muscle was defined as the tetanic stimulated muscle. *P < 0.05 (c-MEP versus p-MEP).

View larger version (12K): [in this window] [in a new window]   Figure 3. Representative conventional motor-evoked potential (c-MEP) (a) and posttetanic MEP (p-MEP) (b) recordings in the same patient without preoperative motor and sensory deficits. For p-MEP recording, tetanic stimulation of the left tibial nerve at the ankle with a duration of 5 s and a stimulus intensity of 50 mA at 50 Hz was performed before transcranial stimulation with a posttetanic interval of 1 s. Note that amplitudes of p-MEPs from the bilateral abductor pollicis brevis (APB), abductor hallucis (AH), tibialis anterior (TA), and soleus (S) muscles were augmented compared with those of c-MEPs.

DISCUSSION

The results of the present study show that the application of tetanic stimulation to the left tibial nerve at the ankle before transcranial stimulation significantly augmented the amplitudes of MEPs recorded from the bilateral APB, AH and S muscles and right TA in patients under propofol and fentanyl anesthesia with partial neuromuscular blockade. Because the left tibial nerve at the ankle mainly innervates only the left AH muscle (TS-muscle), but not other muscles (non-TS muscles), the results indicated that myogenic MEPs from the non-TS muscles, and TS-muscle, were significantly augmented by using p-MEP.

Tetanic stimulation of the peripheral nerve has been widely used as a method to enhance muscle response during neuromuscular blockade.15,16 During the administration of a nondepolarizing neuromuscular blocking drug, tetanic nerve stimulation at 50–100 Hz is followed by a posttetanic increase in twich tension (i.e., posttetanic fasciculation of transmission). The posttetanic count after TS at 50 Hz for 5 s has therefore become an accepted technique to quantify the degree of intense neuromuscular blockade under the conditions in which response to single-twitch stimulation are no longer obtained.17–19 We originally hypothesized that tetanic stimulation of the peripheral nerve before transcranial stimulation may enhance the amplitude of MEPs from the muscles (TS-muscle), which are innervated by the nerve with tetanic stimulation, during the administration of neuromuscular blockade under general anesthesia.

Kakimoto et al.14 investigated whether tetanic stimulation of the peripheral nerve before transcranial electrical stimulation can enlarge amplitudes of MEPs in patients under propofol and fentanyl anesthesia with neuromuscular blockade. They evaluated MEP augmentations by tetanic stimulation at different levels of duration, posttetanic interval, and stimulus intensity. The results indicated that the application of tetanic stimulation to the tibial nerve at a stimulus intensity of 25–50 mA with a duration of 3–5 s and a posttetanic interval of 1–5 s significantly augmented the amplitudes of MEPs to tetanic stimulation from the AH muscle at the ipsilateral side. In the present study, we therefore used tetanic stimulation at a stimulus intensity of 50 mA with a duration of 5 s and a posttetanic interval of 1 s to obtain maximal augmentation of MEPs.

In the report by Kakimoto et al.,14 the application of tetanic stimulation only augmented the MEP amplitudes to tetanic stimulation at the ipsilateral side, but not at the contralateral side. However, after gaining the experience regarding p-MEP recording, we found that MEP amplitudes to tetanic stimulation at the contralateral side were also augmented in addition to the ipsilateral side in some cases. In the current study, we therefore hypothesized that the application of tetanic stimulation of the peripheral nerve before transcranial stimulation might augment the amplitudes of MEPs recorded from the non-TS muscles as well as TS muscle. As a result, tetanic stimulation of the peripheral nerve significantly enhanced MEP amplitudes not only from the TS muscle, but also from non-TS muscles.

The results obtained in this study are contradictory to those of Kakimoto et al.,14 in which tetanic stimulation of the tibial nerve at the ankle augmented MEPs from the TS-muscle, but not from non-TS muscles. The reasons for these contradictory results are unknown. However, one possible explanation is as follows. In the study by Kakimoto et al.,14 patients with preoperative moderate to severe sensory deficits were also enrolled. In contrast, in this study, to exclude any influence of preoperative neurological conditions on MEP augmentations, the patients with preoperative motor dysfunction and moderate to severe sensory deficits were excluded. A patient's profile might therefore have affected the results. In fact, although we did not show the data in this study, our preliminary results showed that preoperative sensory and motor deficits might attenuate the MEP augmentations by the application of tetanic stimulation.

Of interest is that tetanic stimulation of the peripheral nerve before transcranial stimulation augmented the MEPs from non-TS muscles, that is, the phenomenon which induced "remote augmentation of MEPs by peripheral stimulation." To our knowledge, this is the first report to show the remote augmentation of MEPs by tetanic stimulation of the peripheral nerve. The mechanisms of remote augmentations of MEPs are not clear. However, central mechanisms at the levels of spine and brain may be involved in this remote augmentation. Peripheral stimulation has been reported to modulate corticomotoneuronal excitability.20–23 Kaelin-Lang et al.21 demonstrated that ulnar nerve stimulation at the wrist for 2 h enhanced MEP amplitudes to transcranial magnetic stimulation from abductor digiti minimi muscles in humans, and that this effect was blocked by the -aminobutyric acid type A agonist, lorazepam, suggesting that somatosensory stimulation elicited an increase in corticomotoneuronal excitability, probably at the level of the cortex. Andersson and Ohlin23 demonstrated that a train of stimuli to the foot sole within the receptive field of the withdrawal reflex of the TA muscle before transcranial stimulation augmented MEP responses, indicating that the cortically elicited responses were spatially facilitated, probably at the level of the spine. However, further investigations would be required to clarify the mechanisms of MEP augmentations by peripheral nerve stimulation.

There are several limitations to this study. First, only patients without preoperative motor dysfunction and moderate to severe sensory deficits were enrolled. It is, thus, unknown whether remote augmentation of MEPs by peripheral stimulation would be observed in patients with preoperative motor and/or moderate to severe sensory deficits. Second, this study was performed under propofol and fentanyl anesthesia with partial neuromuscular blockade. Although we believe that this is a standard anesthetic regime during the monitoring of MEPs, it is unknown whether remote augmentations of MEPs would be induced under different anesthetic conditions. Third, we used tetanic stimulation at a stimulus intensity of 50 mA with a duration of 5 s and a posttetanic interval of 1 s to obtain maximal augmentation of MEPs, based on the results in the previous study. However, these settings were optimal for augmentation of MEPs from the TS muscle. The optimal setting for augmentation of MEPs from non-TS muscles might be different. Finally, based on the data obtained in the current study, it is unclear whether p-MEPs can really reflect motor function as c-MEPs do. Extensive studies to assess the usefulness of p-MEPs would be required.

In summary, we investigated whether tetanic stimulation of the peripheral nerve before transcranial stimulation can augment myogenic MEPs from non-TS muscles and TS muscle in patients under propofol and fentanyl anesthesia with partial neuromuscular blockade. The results showed that the application of tetanic stimulation before transcranial stimulation induced augmentation of MEPs not only from the TS-muscle, but also from non-TS muscles, indicating "the remote augmentation of MEPs by peripheral stimulation." The relevance of this phenomenon in clinical situations remains undetermined. However, considering that MEP responses are very sensitive to anesthetics and neuromuscular blocking drugs, methods to augment MEP responses are still needed. Because the application of peripheral nerve stimulation at one site enhanced MEP responses from most muscles in the upper and lower limbs, p-MEP may be applied as a method to augment MEP responses for cases in which MEP responses are poor or absent. In addition, transcranial stimulation can induce patient movement, which may put patients at risk of spinal cord, neck, eye, tongue, and lip injury. Yamamoto et al.24 demonstrated that MEP recording was feasible without any patient movement under a deep level of neuromuscular blockade as long as p-MEP was used. Furthermore, the results in this study may provide a key for techniques to augment MEP responses through central facilitation. However, the data concerning clinical validity and usefulness of p-MEP are still limited. To use p-MEP as a routine monitor, further studies would be required.

Footnotes

Accepted for publication March 17, 2008.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Hayashi, H. Articles by Furuya, H. Search for Related Content PubMed PubMed Citation Articles by Hayashi, H. Articles by Furuya, H. Related Collections Obstetrics Monitoring (Non-cardiac) Technology